First Record of the Genus Limnohalacarus (Acari: Halacaridae) from Mexico

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Revista Mexicana de Biodiversidad

Revista Mexicana de Biodiversidad 87 (2016) 1131–1137 www.ib.unam.mx/revista/

Research note

First record of the genus Limnohalacarus (Acari: Halacaridae) from Mexico

Primer registro del género Limnohalacarus (Acari: Halacaridae) de México

a,∗ b c

Margarita Ojeda , Gerardo Rivas , Fernando Álvarez

Colección Nacional de Ácaros, Instituto de Biología, Universidad Nacional Autónoma de México, 3er. Circuito exterior s/n, 04510 Ciudad de México, Mexico

Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Circuito exterior s/n, 04510 Ciudad de México, Mexico

Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado postal 70-153, 04510 Ciudad de México, Mexico

Received 12 January 2016; accepted 4 May 2016

Available online 10 August 2016

Abstract

Limnohalacarus cultellatus Viets, 1940 was collected from an anchialine cave (Cenote Bang) in the Ox Bel Ha system located near Tulum,

Quintana Roo, Mexico. This species has been recorded from the Antilles, Brazil, Hungary, India, Madagascar, El Salvador and USA. The record

presented here is the ﬁrst one of the species for Mexico and the ﬁrst record for an halacarid mite from continental waters in the country. A key to

the species of Limnohalacarus is given as well as information about the variation shown by the organisms named under L. cultellatus.

Creative Commons CC License BY-NC-ND 4.0.

Keywords: Acari; Limnohalacarus; Anchialine; Quintana Roo; First record

Resumen

Limnohalacarus cultellatus Viets, 1940 fue recolectado en una cueva anquihalina (Cenote Bang) del sistema Ox Bel Ha localizado cerca de

Tulum, Quintana Roo, México. La especie se conoce de las Antillas, Brasil, Hungría, India, Madagascar, El Salvador y EUA. El registro que se

presenta es el primero de la especie para México y también el primer reporte de un halacárido en aguas continentales en el país. Se proporciona una

clave para las especies conocidas del género y se aporta información sobre la variación que se observa en los organismos ubicados en L. cultellatus.

bajo los términos de la Licencia Creative Commons CC BY-NC-ND 4.0.

Palabras clave: Acari; Limnohalacarus; Anquihalino; Quintana Roo; Primer registro

Halacaridae are prostigmatid mites with more than 1,100 (MacQuitty, 1983, 1984; Rivas, 2006) and the latter 3 in the

described species around the world (Bartsch, 2009), and as Caribbean Sea (Chatterjee & De Troch, 2001; Krantz, 1971).

a group they are mainly known as the marine mites. Eight This family is mainly marine, occurring at depths ranging

species of halacarids have been reported from Mexico: Agaue from the littoral zone to about 7,000 m (Bartsch, 1988); how-

variabilis MacQuitty, Agauopsis ﬁlirostris MacQuitty, Copidog- ever, some 60 species can be found in continental and coastal

nathus ilsebartschi MacQuitty, Halacarus newelli MacQuitty, fresh and brackish waters (Bartsch, 1996, 2008). In particu-

Simognathus cramerae Rivas, Actacarus giganteus Krantz, lar, the subfamily Limnohalacarinae is composed of 5 genera:

Copidognathus yucatanensis Chatterjee & De Troch, and C. uni- Hamohalacarus Walter, Himejacarus Imamura, Parasoldanel-

custatus Bartsch; the former 5 are distributed along the Paciﬁc lonyx Viets, Soldanellonyx Walter and Limnohalacarus Walter;

all of them with species that inhabit continental waters.

∗ Particularly, the 13 species of Limnohalacarus have a

Corresponding author.

worldwide distribution, living in fresh to slightly brackish

E-mail address: [email protected] (M. Ojeda).

waters (Bartsch, 2013; Pepato & Costa, 2015): Limnohalacarus

Peer Review under the responsibility of Universidad Nacional Autónoma de

México. africanus Walter, L. australis Bartsch, L. capernaumi Petrova,

http://dx.doi.org/10.1016/j.rmb.2016.06.016

Commons CC License BY-NC-ND 4.0.

1132 M. Ojeda et al. / Revista Mexicana de Biodiversidad 87 (2016) 1131–1137

Table 1

Records and variation of the total body size and some of the plates of Limnohalacarus cultellatus.

Distribution Habitat Length/width ratio References

Idiosoma Gnathosoma AD OC PD AE GP

Margarita, Curacao, Piped water, rivers 1.41 1.35 1.00 1.12 1.87 0.80 1.20 Viets (1940)

Aruba and Bonaire and water in ﬁssures

Islands

Andhara Pradesh, Brackish water, bay 1.37 1.42 1.13 1.10 1.92 0.58 1.12 Chatterjee and

India near conﬂuence of a Chang (2005)

river

Georgia and River 1.19 1.65 1.16 1.00 1.78 0.62 0.80 Bartsch (2011)

Wisconsin, USA

Northern Madagascar River, rifﬂe 1.19 NA 1.10 1.10 1.70 NA NA Bartsch (2013)

Rio Grande do Sul, Lake with salinity 1.47 1.28 1.01 1.06 1.53 0.60 0.71 Pepato and

Brazil gradient (brackish to Costa (2015)

freshwater)

Yucatán Peninsula, Anchialine cave 1.34 1.36 1.13 1.53 1.83 0.57 1.17 Present study

Mexico

AD, anterior dorsal plate; AE, anterior epimeral plate; GP, genital plate; NA, not available; OC, ocular plate; PD, posterior dorsal plate.

L. cultellatus Viets, L. dentatus Bartsch, L. fontinalis Walter microscope, cleared in lactic acid and mounted in Hoyer’s

& Bader, L. inopinatus Fain & Lambrechts, L. lanae Green, medium. The illustrations and measurements in micrometers

L. major Bader, L. mamillatus Fain & Lambrechts, L. novus (␮m), were made using a Nikon Optiphot-2 phase contrast

Bartsch, L. portmanni Bader and L. wackeri (Walter). microscope. Microphotographs were obtained with an AxioCam

Only 2 species of Limnohalacarinae have been reported from MRC5 camera using a Carl Zeiss AxioZoom V16 microscope.

the Neotropics. The ﬁrst one, L. cultellatus, originally described The specimen was collected under the scientiﬁc collector’s

from the Antilles, has also published records from the northern license issued to F. Álvarez (FAUT 0104) by the Mexican envi-

USA and El Salvador (Bartsch, 2011), the Caribbean region ronmental authority (Semarnat). The organism was deposited

(Bartsch, 1984; Viets, 1940) and Brazil (Bartsch, 2011; Pepato & in the National Acarological Collection (CNAC) of the Insti-

Costa, 2015). The second species, L. mamillatus, was described tute of Biology, UNAM, México City, with the catalog number

from an aquarium in Belgium and has been recorded in Brazil CNAC009211.

(Pepato & Costa, 2015). The abbreviations used in the diagnosis and redescription

Regarding anchialine systems, only a few records of aquatic are: AD (anterior dorsal plate), AE (anterior epimeral plate), AP

mites exist from caves in Bermuda (Bartsch & Iliffe, 1985). No (anal plate), ds (dorsal setae, from anterior to posterior: ds-1 to

previous records of halacarids exist for the Yucatán Peninsula ds-5), P-2 to P-4 (second to fourth palpal segment), GA (geni-

in Mexico, where large anchialine systems with hundreds of toanal plate), ␧ (famulus), gac (genital acetabula), glp (dorsal or

kilometers of ﬂooded passages have developed. The typical taxa lateral gland pores, from anterior to posterior: glp-1 to glp-5),

occurring in the anchialine systems of Yucatán are crustaceans: GP (genital plate), GO (genital opening), OC (ocular plate), pas

remipedes, amphipods, isopods, ostracods, thermosbaenaceans, (parambulacral seta), PD (posterior dorsal plate), PE (posterior

and caridean shrimps (Álvarez, Iliffe, Benitez, Brankovits, & epimeral plate), pgs (perigenital setae), sgs (subgenital setae),

Villalobos, 2015). ␻ (solenidium), legs (numbered I to IV). Segments, from distal

We herein present a new record of Limnohalacarus cultella- to proximal region are: tarsus, tibia, genu, telofemur, basifemur,

tus from Cenote Bang which is part of the Ox Bel Ha system, and trochanter. The chaetotaxy formulas exclude the solenidia,

Tulum, Quintana Roo, Mexico. The samples of L. cultellatus, famuli and parambulacral setae from the trochanter to the tar-

obtained in 2013 are the ﬁrst for Mexico and also the ﬁrst from sus. The number of bipectinate spines is given in parentheses.

an anchialine habitat. The morphological variations observed Lengths of leg segments are measured along their dorsal margin.

relative to the original description are presented (Table 1), and Measurements are expressed in micrometers (␮m).

an identiﬁcation key for females of all the species of Limnoha-

lacarus is included. Complementary description

The Ox Bel Ha system develops just to the south of the town of Classiﬁcation follows Krantz & Walter, 2009: 98–100.

Tulum, Quintana Roo, Mexico (Fig. 1). Cenote Bang is located Subclass Acari Leach, 1817

in the innermost section of the system about 12 km from the Superorder Acariformes Zakhvatkin, 1952

shore. Around Cenote Bang the submerged galleries develop at Order Trombidiformes Reuter, 1909

an average depth of 18 m and the halocline is present at a depth Superfamily Halacaroidea Cunliffe, 1955

ranging from 18 to 21 m. Family Halacaridae Murray, 1877

Samples were obtained with a plankton net (300 ␮m) from Subfamily Limnohalacarinae Viets, 1927

0 to 8 m in the cenote. The contents were preserved in 70% Genus Limnohalacarus Walter, 1917

ethanol. At the laboratory, mites were sorted under a stereoscopic Limnohalacarus cultellatus Viets, 1940

M. Ojeda et al. / Revista Mexicana de Biodiversidad 87 (2016) 1131–1137 1133

–92º –90º –88º –86º 22º 22º Dos Ojos

0 5 km Gulf of Mexico Xel Ha

HG Yucatan Peninsula Conquistador Mexico Nohoch Nah Chich 20º 20º Tortuga Aktun Ha Casa Cenote Sac Aktun N CV Cenote Bang Abejas Caribbean Esqueloto 18º Sea 18º Laguna La Union TULUM

Guatemala Naranjal Belize Ox Bel Ha Laguna Chumkopo 16º 16º Angelita

Honduras Yaxchen

–92º –90º –88º –86º km Site of collection

0 50 100

Figure 1. Map showing sampling site, Cenote Bang, in the Yucatán Peninsula, Mexico.

Material examined. One female (CNAC 009211), Cenote middle toward the front (Fig. 3A), length 67 ␮m, width 76 ␮m,

◦ ′ ′′

Bang, Tulum, Quintana Roo, Mexico (29 57 30.63 N, length:width ratio 0.9. Medial eye pigment absent, ds-1 on an

◦ ′ ′′

50 09 14.50 W), 4 December 2013, colls. O. Cortes and F. anterior area of AD and ds-2 on membranous cuticle between

Álvarez. AD and OC. OC between slightly rounded and sub-pentagonal,

Diagnosis [according with Viets (1940), Bartsch (2011, 2013) 43 ␮m long, 23 ␮m wide, length:width ratio 1.5, separated from

and Pepato and Costa (2015)]. Length 275–325 ␮m. Dorsal a triangular sclerite, 26 ␮m long, 14 ␮m wide, bearing gland

plates reticulated, except for smooth anteriormost part of AD. pore.

Medial and lateral eye pigment absent. Length: width ratio of Corneas and eye pigment not evident. PD elongated, 218 ␮m

AD 1.0–1.2. OC divided and reticulated, with narrow triangu- long, 119 ␮m wide, 3.2 times longer than AD. PD length:width

lar sclerite bearing gland pore. PD 1.5–2.1 times longer than ratio 1.8. Pairs of glp-4 and glp-5 on striated cuticle lateral to

wide and 2.5 times longer than AD. Second pair of dorsal setae PD. Ventral plates AE, pairs of PE and GP separated by mem-

present. Ventral plates separated. GP with 4–9 pairs of gac, 3, branous cuticle. AE 116 ␮m long, 215 ␮m wide, with 3 pairs of

rarely 4, pairs of pgs and 2 pairs of sgs. Gnathosoma 1.3–1.5 ventral setae, PE with 3 setae. GP 162 ␮m long, 138 ␮m wide,

times longer than wide; rostrum slender. Both pairs of maxillary with 3 pairs of pgs and 11–14 gac, GO in posterior part of ven-

setae slender. Pharyngeal plate removed from margin of gnatho- tral shield (Fig. 3B). Genital sclerites large, 68 ␮m long, 31 ␮m

somal base by more than half its length. P-2 basally abruptly wide, with 2 pairs of sgs. Length of gnathosoma 97 ␮m, width

widened, in lateral view rectangular with straight dorsal margin. 71 ␮m, gnathosoma length:width ratio 1.36; rostrum (Fig. 2C),

Telofemur I, 1.6–1.8 times longer than wide. Tarsi with spini- 40 ␮m long, equal to 0.41 of gnathosoma length. Dorsal and

form lamellae near bases. Trochanters I–IV with 1, 1, 1, 1 setae, basal pairs of maxillary setae slender (Fig. 3C). Dorsal mar-

basifemora with 4, 3, 2, 1 setae, genua III with 4 setae, and tib- gin of P-2 straight (Fig. 3D). Legs slender (Figs. 2D, 3E–H).

iae I–IV with 7, 6, 7, 6 setae. On tibiae I–III, 1, 1, 2 pectinate Length/height of telofemora I–IV: 2.6, 1.8, 1.7, 1.7 times, respec-

setae, on tibia IV all setae slender. Tibiae III and IV with 4 and tively. Telofemur/tibia length ratio I–IV: 0.99, 0.94, 0.66, 0.60.

3 ventral setae, respectively. All tarsi with pairs of pas singlets. Leg chaetotaxy from trochanter to tarsus (solenidia, famuli and

Claws on tarsus I slender, claws with lamellar basal process parambulacral setae excluded): I: 1, 4, 4, 6, 7(I), 4; II: 1, 3, 4, 6,

and delicate apical tines. Claws of tarsi II–IV with series of 6(I), 3; III: 1, 2, 3, 4, 7(II), 4; IV: 1, 1, 3, 3, 6, 3. Tibia III with

tines from apical accessory process to basal process. Male: not 2 bipectinate ventromedial and 2 slender and smooth ventrolat-

known. eral setae. All tarsi with pairs of pas singlets. Claw I with long

Redescription. Female. Idiosoma 329 ␮m long, 245 ␮m wide tines arranged along inner ﬂank and distal outer portion of claw

(Fig. 2A). Dorsal plates reticulated (Fig. 2B). AD hexagonal, (Fig. 3I). Claws on tarsi II–IV with tines and a developed basal

posterior border truncate, 1 small anterior projection in the lamellar process.

1134 M. Ojeda et al. / Revista Mexicana de Biodiversidad 87 (2016) 1131–1137

Figure 2. Limnohalacarus cultellatus Viets, 1940, female: A, habitus; B, idiosoma, dorsal plates; C, gnathosoma; D, legs I and II.

The habitat of Halacaridae has been mainly in the marine Pepato and Costa (2015), and Viets (1940), for Limnohalacarus

environment, which is interpreted as a successful secondary cultellatus; the main measurements of the specimen are within

adaptation from their terrestrial prostigmads ancestors (Bartsch, the recorded range based on records given for the species around

1989). The fact that around 5% of halacarid mites live in conti- the world. In addition to the original description by Viets (1940)

nental waters raise interesting questions of how they were able for L. cultellatus, 9 records, including the one presented here

to invade freshwater habitats and how the ways of life played from the Yucatán Peninsula are known (Table 1). All of these

a role in this process (Bartsch, 1996; Delamare-Deboutteville, are almost always based on 1 or 2 individuals, and because of

1960). The evolutionary pathways of marine groups to fresh- this limited number an assessment of the morphological varia-

waters through subterranean systems implies interactions with tion is difﬁcult to obtain, it has yet to be established if it is a wide

hydrogeological processes at different scales (Ward & Palmer, ranging species with a signiﬁcant degree of morphological vari-

1994), aspects to consider for the invertebrate fauna of anchialine ation or a species complex, that in the future could be resolved

systems. incorporating molecular information about these mites. Accord-

The halacarid recently collected from Cenote Bang ﬁt well the ing to Bartsch (2013), L. cultellatus, L. australis (Australia), and

diagnostic characteristics established by Bartsch (2011, 2013), L. inopinatus (Aquarium in Belgium) are members of the same

M. Ojeda et al. / Revista Mexicana de Biodiversidad 87 (2016) 1131–1137 1135

Figure 3. Limnohalacarus cultellatus Viets, 1940, female: A, idiosoma, dorsal view; B, idiosoma, ventral view; C, gnathosoma, ventral view; D, pedipalp, lateral

view (scale bar = 20 ␮m); E, leg I; F, leg II; G, leg III; H, leg IV; I, tarsus I. Scale bars = 50 ␮m.

clade. The differences observed between these species in the PD necessary to answer questions about the delimitation of the

length: width ratio, the number of apical tines on claws I, and species as well as to understand the diversiﬁcation pro-

presence of rather thick, barbed setae on tibia IV could be inter- cess.

preted as intraspeciﬁc variation and not as a variation between The third author gratefully acknowledges the funding

2 species. awarded though a Conacyt grant 155644(546) “Processes that

The species of Limnohalacarus have a cosmopolitan distri- create and maintain the biodiversity in an extreme environment:

bution in spite of not having efﬁcient dispersal mechanisms. the anchialine systems of Yucatán”. We appreciate the assistance

However, it is thought that the combination of an ancient provided by Drs. Ilse Bartsch and Almir Pepato with part of the

radiation to freshwater since the Mesozoic and the possi- literature cited. We would also like to thank Olinka Cortes for

ble parthenogenetic mode of reproduction of some of the obtaining the samples and Susana Guzmán from IBUNAM for

species could contribute to their wide geographical distribu- the technical assistance in taking the microphotographs. We also

tion (Bartsch, 1996, 2008). The efforts to study halacarid thank the two anonymous reviewers for their contributions to the

mites in environments such as the anchialine caves are manuscript.

1136 M. Ojeda et al. / Revista Mexicana de Biodiversidad 87 (2016) 1131–1137

Key for females of all the known species of Limnohalacarus.

1a. Gland pores (glp) within OC, ventral plate fused…………...... ………………...... 2 1b. Gland pores (glp) outside OC, ventral plates separated ……...... 8

2a. Gnathosoma length:width ratio 1.0 to 1.2……...... ……………...... …...... 3

2b. Gnathosoma length:width ratio 1.3 to 1.7 ……...... ………...... ………...... L. major

3a. 0-1 subgenital setae………...... ………………………………………………………4

3b. 2 or more subgenital setae …………………………...... …...... ……………………………… …5

4a. Apical maxillary setae wide ……...... …………………………………..….……. … L. lanae

4b. Apical maxillary setae slender…...... ………………………….……. …. ….….L. mamillatus

5a. 4 or more small tines on claws III and IV ……...... ………………………………….…… …6

5b. 2 strong tines on claws III and IV …...... …………………………….…….…… … L. dentatus

6a. Length of idiosoma less than 300 μm……...... ………………….…………...... ………. . …. .. .7

6b. Length of idiosoma higher than 300 μm……..…………...... ……….…...…..… .…L. fontinalis

7a. AD lenght/width 0.9 and OC lenght/widht 1.4 or more ……...... ……...….… …. …… L. novus

7b. A D length/width 0.7 and OC less than 1.4……...... … …………..……...……..… L. portmanni

8a. Parambulacral setae of leg I doublets ……...... ……………………..……………………… …9

8b. Parambulacral setae of leg I singlets ………...... ……………………..……….…….… …11

9a. 5 or more perigenital setae ………...... …………………………………….. … …… … …10

9b. 3-4 perigenital setae ………………………………………...... ….…….…… … L. africanus

10a. Eye pigment and / or cornea absent …………………………...... …..... …..... L. capernaumi

10b. Eye pigment and / or cornea present ………...... ……………… … ….. … …...... L. wackeri

11a. Tibia IV with 1 pectinate spiniform setae …………...... …….……… ………L. inopinatus

11b. Tibia IV without pectinate spiniform setae ………...... ……………….………….……12

12a. AD completely reticulated ……………...... …………………….…… …… … L. australis

12b. AD reticulated, except anterior most part……...... ………………… ..…..…… ..……L. cultellatus

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